Lorraine Olendzenski

Horizontal transfer of archaeal genes into the deinococcaceae: detection by molecular and computer-based approaches.

Abstract. Members of the Deinococcaceae (e.g., Thermus, Meiothermus, Deinococcus) contain A/V-ATPases typically found in Archaea or Eukaryotes which were probably acquired by horizontal gene transfer. Two methods were used to quantify the extent to which archaeal or eukaryotic genes have been acquired by this lineage. Screening of a Meiothermus ruber library with probes made against Thermoplasma acidophilum DNA yielded a number of clones which hybridized more strongly than background. One of these contained the prolyl tRNA synthetase (RS) gene. Phylogenetic analysis shows the M. ruber and D. radiodurans prolyl RS to be more closely related to archaeal and eukaryal forms of this gene than to the typical bacterial type. Using a bioinformatics approach, putative open reading frames (ORFs) from the prerelease version of the D. radiodurans genome were screened for genes more closely related to archaeal or eukaryotic genes. Putative ORFs were searched against representative genomes from each of the three domains using automated BLAST. ORFs showing the highest matches against archaeal and eukaryotic genes were collected and ranked. Among the top-ranked hits were the A/V-ATPase catalytic and noncatalytic subunits and the prolyl RS genes. Using phylogenetic methods, ORFs were analyzed and trees assessed for evidence of horizontal gene transfer. Of the 45 genes examined, 20 showed topologies in which D. radiodurans homologues clearly group with eukaryotic or archaeal homologues, and 17 additional trees were found to show probable evidence of horizontal gene transfer. Compared to the total number of ORFs in the genome, those that can be identified as having been acquired from Archaea or Eukaryotes are relatively few (approximately 1%), suggesting that interdomain transfer is rare.

Gene duplications and horizontal gene transfer during early evolution

The evolutionary history of organisms can be reconstructed using various information sources: the fossil and geological records, the comparative analysis of biochemical pathways, and the reconstruction of molecular phylogenies from macromolecules found in extant organisms. In the absence of a complete archaean microfossil record and unique morphological characters for most microbial groups, molecular markers have been used to unravel the relationships between the major groups ofprokaryotes. The best studied of these molecules is undoubtedly the small subunit ribosomal RNA, but many other macromolecules, especially protein sequences have been useful in studying the relationships among prokaryotic kingdoms and domains. However, at best, the analysis of extant macromolecules can only yield information on tile phylogeny of the molecules under study. Even if molecular phylogenies could be resolved without ambiguity, the step from molecular phylogeny to species phylogeny would remain complicated because genetic information has also been transferred horizontally between independent evolutionary lineages. It is therefore not surprising that comparative analysis of different molecular phylogenies reveals a net-like structure of the species phylogeny (Gogarten, 1995; Hiliario & Gogarten, 1993). Differences between well resolved molecular phylogenies can be due either to unrecognized gene duplications or to horizontal gene transfer. Two examples that conflict with well documented phylogenetic relationships are the presence of archaeal type H+-ATPases in Thermus and Enterococcus and the close association between Gram positive eubacteria and archaea as supported by many different genes, including heat shock proteins (HSP70), ghitamine synthetases and glutamate dehydrogenases. In both cases the best explanation for these conflicts is horizontal gene transfer. Assuming unrecognized paralogies (duplicated genes) as an explanation would necessitate many instances of convergent evolution; furthermore this assumption would also result in species phylogenies that are at odds with two distinct prokaryotic domains (archaea and eubacteria). The large number of characters that reflect the close association between archaea and eubacteria suggest that a substantial portion of the eubacterial genome participated in this transfer. Horizontal gene transfer as a possible evolutionary mechanism gives as a result net-like species phylogenies that complicate inferring the properties of the last common ancestor. Even so, the data strongly indicate that the last common ancestor was a cellular organism, with a DNA based genome, and a sophisticated transcription and translation machinery. Furthermore, the analysis of ATPase structure function relationships and the evolution of cytochrome oxidase homologues suggest that the last

Evolution of Genes and Organisms

Gene exchange necessitates expanding the model of the tree of life, impacts the notion of organismal and molecular most recent common ancestors, and provides examples of natural selection working at multiple levels. Gene exchange, whether by horizontal gene transfer (HGT), hybridization of species, or symbiosis, modifies the organismal tree of life into a web. Darwin suggested the tree of life was like a coral, where living surface branches were supported by masses of dead branches. In phylogenetic trees, organismal or molecular lineages coalesce back to a lucky universal ancestor whose descendents are found in current lineages and which coexisted with other, now‐extinct lineages. HGT complicates the reconstruction of a universal ancestor; genes in a genome can have different evolutionary histories, and even infrequent gene transfer will cause different molecular lineages to coalesce to molecular ancestors that existed in different organismal lineages and at different times. HGT, as well as symbiosis, provides a mechanism for integrating and expanding the organizational level on which natural selection acts, contributing to selection at the group and community level.

Horizontal Gene Transfer: Pitfalls and Promises

J. PETER GOGARTEN, RYAN D. MURPHEY, AND LORRAINE OLENDZENSKI Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269-3044 Phylogenetic reconstruction from protein or nucleic acid sequence families provides information on the evolution of individual genes. In contrast to the assumed bifurcating, tree-like evolution of genes, organismal evolution is char- acterized by the exchange of genetic information between organisms and even by the fusion of formerly independent lines of descent (1). The invocation of horizontal gene transfer events is often regarded as a last-ditch attempt by systematists to reconcile conflicting phylogenies con- structed from different markers. In general, however, organ- ismal evolution is clearly visible as the majority consensus of a number of molecular phylogenies, and transfer events can be recognized in phylogenies constructed from one or several markers whose topologies deviate from that of the consensus. Often it is difficult to decide whether conflicts between molecular phylogenies are due to actual events in evolution (horizontal gene transfer or gene duplications [see 2]), or due to artifacts generated during phylogenetic reconstruc- tion. For example, investigation of the maximum likelihood landscape of 18s rRNA and V-ATPase A-subunit phylog- enies suggests that the grouping of microsporidia either with the fungi (3,4,5) or close to the root of the archaeal domain (e.g., 6, 7, 8) probably represents an artifact in the 18s rRNA data analyses and not another case of horizontal transfer. Although the recognition of horizontal transfer as a major factor in prokaryotic evolution (e.g., 9, 10, 11, 12) certainly complicates the interpretation of molecular phylogenies, it also allows synchronization of different parts of the univer- sal tree of life, and thus might provide the key to the detection of periods of rapid substitutions. Two examples

Horizontal Gene Transfer

In this paper the conception of horizontal gene transfer (HGT) was introduced,and main mode of HGT was also enumerated as follows: HGT by medium such as plasmid and virus etc., and the HGT without any medium. The transfer of genes from one species to another especially between remote species was emphasized by the information from genome sequencing. The problems about evolution phylogenies and safety of GEMs (gene engineered microorganisms) for HGT were discussed.

Horizontal Gene Transfer: A New Taxonomic Principle?

Publisher Summary The important role of horizontal gene transfer (HGT) in the spread of antibiotic resistance, the formation of pathogenicity islands, and selfish genes has long been established. HGT also has been suggested as a major force in structuring prokaryotic genomes, e.g. Lawrence and Roths selfish operon theory. The fact that HGT occurred is no longer disputed; however, the impact of HGT on microbial evolution, in particular, on the ability to reconstruct organismal evolutionary history, remains controversial. This isolation with respect to HGT could either be caused by an environment that is less conducive to HGT or by physiological or genetic isolating mechanisms that evolve within the organisms. The horizontal transfer of genes and their complete uninterrupted incorporation into the genome of the recipient lead to a mosaic genome where different parts of the genome reflect different histories. It is clear that both vertical inheritance and horizontal transfer have played a role in microbial evolution.

Gene Transfer: Who Benefits?

Horizontal gene and genome transfer forces us to recognize that life evolves by fusion as well as bifurcation of lineages, and necessitates the expansion of traditional views of evolution. This chapter reviews the role that horizontal gene transfer (HGT) may play in integrating selection at the gene, species, and community levels. Additionally, we provide an overview of the structure and content of this book, which reflects current thought in the dynamic field of HGT research.

Chapter 34 – Horizontal Gene Transfer: A New Taxonomic Principle?

Publisher Summary The important role of horizontal gene transfer (HGT) in the spread of antibiotic resistance, the formation of pathogenicity islands, and selfish genes has long been established. HGT also has been suggested as a major force in structuring prokaryotic genomes, e.g. Lawrence and Roths selfish operon theory. The fact that HGT occurred is no longer disputed; however, the impact of HGT on microbial evolution, in particular, on the ability to reconstruct organismal evolutionary history, remains controversial. This isolation with respect to HGT could either be caused by an environment that is less conducive to HGT or by physiological or genetic isolating mechanisms that evolve within the organisms. The horizontal transfer of genes and their complete uninterrupted incorporation into the genome of the recipient lead to a mosaic genome where different parts of the genome reflect different histories. It is clear that both vertical inheritance and horizontal transfer have played a role in microbial evolution.

Gene Transfer in Early Evolution

Clues to the early evolutionary history of microorganisms can be found in the macromolecules of extant organisms. Two types of molecular data have proven useful in the study of early evolution: comparative analysis of biochemical pathways (Wachtershauser, 1992, Morowitz, 1992) and analysis of macromolecular sequence data. Universal phylogenies inferred from nucleic acid or amino acid sequences which compare organisms from distant lineages allow us to infer major events in the early history of life. Burgeoning data available from molecular databases and ongoing genome projects now allow us to examine phylogenies from many different molecular markers. However, phylogenies from different markers do not always yield the same branching pattern. Rather, markers can be grouped into categories that show a concensus relationship, or into those that show conflicting topology.